Molecular Exploration of Bioavailable Dissolved Organic Matter Across Aquatic Ecosystems

168 Pages·2017·4.9 MB·English

by  Yuan Shen

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Theses and Dissertations
2017
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Yuan Shen
University of South Carolina
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Shen, Y.(2017). Molecular Exploration of Bioavailable Dissolved Organic Matter Across Aquatic
Ecosystems. (Doctoral dissertation). Retrieved from https://scholarcommons.sc.edu/etd/4231
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MOLECULAR EXPLORATION OF BIOAVAILABLE DISSOLVED ORGANIC MATTER
ACROSS AQUATIC ECOSYSTEMS

by

Yuan Shen

Bachelor of Science
Xiamen University, 2009

Master of Science
University of South Carolina, 2011

Submitted in Partial Fulfillment of the Requirements

For the Degree of Doctor of Philosophy in

Marine Science

College of Arts and Sciences

University of South Carolina

2017

Accepted by:

Ronald Benner, Major Professor

James Pinckney, Committee Member

Lori Ziolkowski, Committee Member

Karl Kaiser, Committee Member

Cheryl L. Addy, Vice Provost and Dean of the Graduate School
© Copyright by Yuan Shen, 2017
All Rights Reserved.
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DEDICATION
I would like to dedicate this dissertation to my wife Jiani Zheng and my parents
for all their love and support.
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ACKNOWLEDGEMENTS
I would like to express my deepest appreciation to my advisor, Professor Ronald
Benner, for his guidance, patience, encouragement, and support. His enthusiasm, vision,
and creative thinking have been a great influence on me throughout my graduate studies.
He made every project that we worked together so much enjoyable. One could not ask for
a better advisor. I thank James Pinckney, Lori Ziolkowski, and Karl Kaiser for being on
my committee and providing helpful comments and suggestions. I am very much
thankful to Karl Kaiser and Cédric Fichot for teaching me the amino acid analysis and the
DOC and CDOM analyses, respectively. I also thank my other lab mates and colleagues,
Mike Philben, Oliver Lechtenfeld, Shengkang Liang, Qinghui Huang, Dandan Duan,
Tae-Hoon Kim, Doug Bell, etc. for their companionship and the fun chatting on science
and life. Special thanks go to my friends at the Gamecock Badminton Club (Richard
Cheng, Xinyu Huang, Xinfeng Liu, Jo Evaristo, Xiaolong Liu, etc.), I appreciate their
friendship and the good times that we spent together making my journey more joyful and
memorable. Finally, I thank my collaborators for their contributions to this work and the
US National Science Foundation for funding my research.

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ABSTRACT
Dissolved organic matter (DOM) in aquatic ecosystems is a large reservoir of
reduced carbon that is mostly resistant to degradation. A small fraction of DOM cycles
relatively quickly and is biologically utilized on timescales of days to months. This
bioavailable DOM (BDOM) supports aquatic food webs, drives major elemental cycles,
and is coupled to atmospheric CO . Despite wide-ranging importance, bioavailability of
2
DOM and its linkages to ecosystem properties (e.g., primary production, nutrients) are
poorly characterized, particularly at the ecosystem level. Bioassay experiments are
commonly used to determine BDOM, but this approach alters conditions and has limited
spatial and temporal coverage. In this dissertation, biochemical indicators of DOM
bioavailability were developed and implemented in a wide range of ecosystems to reveal
large-scale distributions of BDOM in the Arctic (Chapter 1) and Antarctic Oceans
(Chapter 2), locate seasonal biological hotspots in a subtropical ocean margin (Chapter
3), and to trace transport and fate of BDOM from surface to ground waters (Chapter 4).
Measurements of amino acids, a major bioactive component of BDOM, were
compared between the high (Chukchi Sea) and low (Beaufort Sea) productivity regions of
the western Arctic Ocean. Bulk concentrations of dissolved organic carbon (DOC) were
similar in the two systems despite their contrasting productivity, but DOM bioavailability
as indicated by amino acid yields was much higher in the more productive Chukchi Sea.
Seasonal trends of amino acids revealed elevated production and rapid off-shelf transport
of BDOM in the Chukchi Sea during a season with reduced sea-ice cover.
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The use of amino acids as BDOM indicator was further tested in the Southern
Ocean during austral winter when primary production is light-limited and minimal. The
sampling encompassed ice-covered and ice-free waters along a latitudinal gradient in the
region of the Antarctic Peninsula, one of the fastest warming regions on Earth. Unlike the
DOC that varied irregularly, amino acid-based indices illustrated a significant northward
increase in DOM bioavailability from ice-covered to open waters. Overall, the
observations in the polar oceans indicate a correspondence between DOM bioavailability
and nutrient- and light-driven changes in ecosystem productivity.
A novel approach using two biochemical indicators (amino acids and
carbohydrates) of BDOM was developed during a large-scale seasonal survey of the
river-influenced Louisiana margin. These indicators revealed patchy distributions of
compositionally distinct types of BDOM hotspots that varied with phytoplankton biomass
and nutrient levels, and they further indicated a diel variability in sources of BDOM, with
zooplankton grazing at night and phytoplankton extracellular release during daytime
under nutrient limitation.
Biochemical indicators were extended to surface and groundwater in South
Carolina. Amino acids, lignin phenols, and chromophoric DOM were monitored monthly
over two years. Linking groundwater DOM with surface water DOM and precipitation
revealed differential transport of hydrophilic and hydrophobic molecules through soils
and depletion of BDOM in groundwater. These observations guided a development of the
Regional Chromatography Model to illustrate processes regulating the composition and
bioavailability of DOM during transport through the soil column to the saturated zone.
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TABLE OF CONTENTS
DEDICATION ....................................................................................................................... iii
ACKNOWLEDGEMENTS ........................................................................................................ iv
ABSTRACT ............................................................................................................................v
LIST OF TABLES ................................................................................................................ viii
LIST OF FIGURES ................................................................................................................. ix
LIST OF ABBREVIATIONS ..................................................................................................... xi
CHAPTER 1: DISSOLVED ORGANIC MATTER COMPOSITION AND BIOAVAILABILITY REFLECT
ECOSYSTEM PRODUCTIVITY IN THE WESTERN ARCTIC OCEAN ............................................1

CHAPTER 2 BIOAVAILABLE DISSOLVED ORGANIC MATTER AND BIOLOGICAL HOT SPOTS
DURING AUSTRAL WINTER IN ANTARCTIC WATERS ..........................................................29

CHAPTER 3 BIOLOGICAL HOT SPOTS AND THE ACCUMULATION OF MARINE DISSOLVED
ORGANIC MATTER IN A HIGHLY PRODUCTIVE OCEAN MARGIN ........................................54

CHAPTER 4 ORIGINS AND BIOAVAILABILITY OF DISSOLVED ORGANIC MATTER IN
GROUNDWATER ..................................................................................................................86

CHAPTER 5 OVERVIEW AND SYNTHESIS ...........................................................................120

REFERENCES .....................................................................................................................123
APPENDIX A – SUPPLEMENTARY TABLES .........................................................................143
APPENDIX B – SUPPLEMENTARY FIGURES ........................................................................144
APPENDIX C – PERMISSION TO REPRINT ...........................................................................146

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LIST OF TABLES
Table 1.1 Physicochemical characteristics in the Chukchi and Beaufort Seas .................19
Table 1.2 Comparisons of concentrations of DOC and TDAA, and TDAA yields ..........20
Table 1.3 Comparisons of concentrations of DOC and TDAA, and TDAA yields ..........21
Table 2.1 Summary of oceanographic parameters at the sampling stations ......................46
Table 2.2 Physicochemical properties of water masses and biological hotspots ..............47
Table 3.1 Average values and ranges for DOC, TDAA, and TDNS in the mixed layer
during the five cruises on the Louisiana margin ................................................................75

Table 3.2 Concentrations and compositions of DOM during the shipboard bioassays .....76
Table 3.3 Surface mixed layer reservoirs of DOC on the Louisiana shelf .......................77

Table 4.1 DOC and amino acids in ground and surface waters and freshly-produced
bacterial DOM .................................................................................................................106

Table 4.2 Optical properties of DOM in ground and surface waters ...............................108
Table 4.3 Correlation matrix between precipitation and DOM in groundwater ..............109
Table 4.4 Lignin phenols in ground and surface waters ..................................................110
Table 4.5 Yields of D-amino acids in freshly-produced bacterial DOM ........................111

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LIST OF FIGURES
Figure 1.1 Locations of sampling stations in the western Arctic Ocean ...........................22
Figure 1.2 Mixing patterns of DOM in the Mackenzie River plume ................................23
Figure 1.3 Concentrations of DOC in the Chukchi Sea and Beaufort Sea ........................24
Figure 1.4 Concentrations of TDAA in the Chukchi Sea and Beaufort Sea .....................25
Figure 1.5 DOC-normalized yields of TDAA in the Chukchi Sea and Beaufort Sea .......26
Figure 1.6 Average concentrations of DOC and TDAA, and TDAA yields in the Chukchi
and Beaufort Seas ..............................................................................................................27

Figure 1.7 Average concentrations of DOC and TDAA, and TDAA yields in the Chukchi
Sea between 2002 and 2004 ...............................................................................................28

Figure 2.1 Sampling sites off the South Shetland Islands (Antarctica) in August 2012 ...48
Figure 2.2 Distributions of temperature and salinity ........................................................49
Figure 2.3 Latitudinal distributions of chl-a and POC in different water masses .............50
Figure 2.4 Latitudinal distributions of DOC and TDAA in different water masses .........51
Figure 2.5 Profiles of chl-a, DOC, TDAA and POC at ice-free and ice-covered stations 52
Figure 2.6 Depth profiles of TDAA yields, glycine, nonprotein amino acids, and D-amino
acids at four ice-free stations .............................................................................................53

Figure 3.1 Study area and sampling sites on the Louisiana margin ..................................78
Figure 3.2 Seasonal and spatial distributions of DOC, TDAA, and TDNS ......................79
Figure 3.3 Seasonal distributions of TDAA and TDNS yields .........................................80
Figure 3.4 Hot spots of labile DOM on the Louisiana margin ..........................................81
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